Identifying apicoplast-targeting antimalarials using high-throughput compatible approaches

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3583-3593

  Ekland, Eric H ^a   Schneider, Jessica ^a   Fidock, David A ^a  

^a Hammer Health Sciences Center ^*  (United States)

Author keywords

Delayed death; Drug discovery; Plasmodium falciparum

Indexed keywords

5 METHOXY 3 (1,2,3,6 TETRAHYDRO 4 PYRIDYL) 1H INDOLE; ANTIMALARIAL AGENT; AZITHROMYCIN; CHLOROQUINE; FLUPHENAZINE; KITASAMYCIN; MACROLIDE; NUCLEIC ACID; OXICONAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL ACTIVITY; APICOPLAST; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG POTENCY; FIREFLY; FLOW CYTOMETRY; HIGH THROUGHPUT SCREENING; IC 50; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; MOLECULAR IMAGING; MOUSE; NONHUMAN; PARASITE; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROGENY; REPORTER GENE; VITAL STAIN;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMALARIALS; DRUG EVALUATION, PRECLINICAL; MICE; ORGANELLES; PARASITEMIA; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII; REPRODUCIBILITY OF RESULTS;

MURINAE; PLASMODIUM FALCIPARUM;

EID: 80053912304     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-187401     Document Type: Article

References (59)

1. Aregawi, M., Cibulskis, R., Kita, Y., Otten, M., and Williams, R. (2010) World Malaria Report 2010, p. xii, World Health Organization, Geneva, Switzerland
2. Plowe, C. V. (2009) The evolution of drug-resistant malaria. Trans. R. Soc. Trop. Med. Hyg. 103(Suppl. 1), S11-S14
3. Eastman, R. T., and Fidock, D. A. (2009) Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria. Nat. Rev. Microbiol. 7, 864-874
4. Noedl, H., Se, Y., Schaecher, K., Smith, B. L., Socheat, D., and Fukuda, M. M. (2008) Evidence of artemisinin-resistant malaria in western Cambodia. N. Engl. J. Med. 359, 2619-2620
5. Dondorp, A. M., Nosten, F., Yi, P., Das, D., Phyo, A. P., Tarning, J., Lwin, K. M., Ariey, F., Hanpithakpong, W., Lee, S. J., Ringwald, P., Silamut, K., Imwong, M., Chotivanich, K., Lim, P., Herdman, T., An, S. S., Yeung, S., Singhasivanon, P., Day, N. P. J., Lindegardh, N., Socheat, D., and White, N. J. (2009) Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 361, 455-467
6. Silvie, O., Mota, M. M., Matuschewski, K., and Prudencio, M. (2008) Interactions of the malaria parasite and its mammalian host. Curr. Opin. Microbiol. 11, 352-359
7. Greenwood, B. M., Fidock, D. A., Kyle, D. E., Kappe, S. H., Alonso, P. L., Collins, F. H., and Duffy, P. E. (2008) Malaria: progress, perils, and prospects for eradication. J. Clin. Invest. 118, 1266-1276
8. Gamo, F.-J., Sanz, L. M., Vidal, J., de Cozar, C., Alvarez, E., Lavandera, J.-L., Vanderwall, D. E., Green, D. V. S., Kumar, V., Hasan, S., Brown, J. R., Peishoff, C. E., Cardon, L. R., and Garcia-Bustos, J. F. (2010) Thousands of chemical starting points for antimalarial lead identification. Nature 465, 305-310
9. Guiguemde, W. A., Shelat, A. A., Bouck, D., Duffy, S., Crowther, G. J., Davis, P. H., Smithson, D. C., Connelly, M., Clark, J., Zhu, F., Jiménez-Díaz, M. B., Martinez, M. S., Wilson, E. B., Tripathi, A. K., Gut, J., Sharlow, E. R., Bathurst, I., El Mazouni, F., Fowble, J. W., Forquer, I., McGinley, P. L., Castro, S., Angulo-Barturen, I., Ferrer, S., Rosenthal, P. J., Derisi, J. L., Sullivan, D. J., Lazo, J. S., Roos, D. S., Riscoe, M. K., Phillips, M. A., Rathod, P. K., Van Voorhis, W. C., Avery, V. M., and Guy, R. K. (2010) Chemical genetics of Plasmodium falciparum. Nature 465, 311-315
10. Rottmann, M., McNamara, C., Yeung, B. K., Lee, M. C., Zou, B., Russell, B., Seitz, P., Plouffe, D. M., Dharia, N. V., Tan, J., Cohen, S. B., Spencer, K. R., Gonzalez-Paez, G. E., Lakshminarayana, S. B., Goh, A., Suwanarusk, R., Jegla, T., Schmitt, E. K., Beck, H. P., Brun, R., Nosten, F., Renia, L., Dartois, V., Keller, T. H., Fidock, D. A., Winzeler, E. A., and Diagana, T. T. (2010) Spiroindolones, a potent compound class for the treatment of malaria. Science 329, 1175-1180
11. Baniecki, M. L., Wirth, D. F., and Clardy, J. (2007) High-throughput Plasmodium falciparum growth assay for malaria drug discovery. Antimicrob. Agents Chemother. 51, 716-723
12. Stanway, R. R., Witt, T., Zobiak, B., Aepfelbacher, M., and Heussler, V. T. (2009) GFP-targeting allows visualization of the apicoplast throughout the life cycle of live malaria parasites. Biol. Cell 101, 415-430
13. Kalanon, M., and McFadden, G. I. (2010) Malaria, Plasmodium falciparum and its apicoplast. Biochem. Soc. Trans. 38, 775-782
14. Ralph, S. A., van Dooren, G. G., Waller, R. F., Crawford, M. J., Fraunholz, M. J., Foth, B. J., Tonkin, C. J., Roos, D. S., and McFadden, G. I. (2004) Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2, 203-216
15. Zuther, E., Johnson, J. J., Haselkorn, R., McLeod, R., and Gornicki, P. (1999) Growth of Toxoplasma gondii is inhibited by aryloxyphenoxypropionate herbicides targeting acetyl-CoA carboxylase. Proc. Natl. Acad. Sci. U. S. A. 96, 13387-13392
16. Dahl, E. L., Shock, J. L., Shenai, B. R., Gut, J., Derisi, J. L., and Rosenthal, P. J. (2006) Tetracyclines specifically target the apicoplast of the malaria parasite Plasmodium falciparum. Antimicrob. Agents Chemother. 50, 3124-3131
17. Goodman, C. D., Su, V., and McFadden, G. I. (2007) The effects of anti-bacterials on the malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 152, 181-191
18. Sidhu, A. B. S., Sun, Q., Nkrumah, L. J., Dunne, M. W., Sacchettini, J. C., and Fidock, D. A. (2007) In vitro efficacy, resistance selection, and structural modeling studies implicate the malarial parasite apicoplast as the target of azithromycin. J. Biol. Chem. 282, 2494-2504
19. Dharia, N. V., Plouffe, D., Bopp, S. E., Gonzalez-Paez, G. E., Lucas, C., Salas, C., Soberon, V., Bursulaya, B., Kochel, T. J., Bacon, D. J., and Winzeler, E. A. (2010) Genome scanning of Amazonian Plasmodium falciparum shows subtelomeric instability and clindamycin-resistant parasites. Genome Res. 20, 1534-1544
20. Dahl, E. L., and Rosenthal, P. J. (2008) Apicoplast translation, transcription and genome replication: targets for antimalarial antibiotics. Trends Parasitol. 24, 279-284
21. Istvan, E. S., Dharia, N. V., Bopp, S. E., Gluzman, I., Winzeler, E. A., and Goldberg, D. E. (2011) Validation of isoleucine utilization targets in Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 108, 1627-1632
22. Nkrumah, L. J., Muhle, R. A., Moura, P. A., Ghosh, P., Hatfull, G. F., Jacobs, W. R., and Fidock, D. A. (2006) Efficient sitespecific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat. Meth. 3, 615-621
23. Muhle, R. A., Adjalley, S., Falkard, B., Nkrumah, L. J., Muhle, M. E., and Fidock, D. A. (2009) A var gene promoter implicated in severe malaria nucleates silencing and is regulated by 3′untranslated region and intronic cis-elements. Int. J. Parasitol. 39, 1425-1439
24. Waller, R. F., Reed, M. B., Cowman, A. F., and McFadden, G. I. (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19, 1794-1802
25. Ekland, E. H., and Fidock, D. A. (2008) In vitro evaluations of antimalarial drugs and their relevance to clinical outcomes. Int. J. Parasitol. 38, 743-747
26. Plouffe, D., Brinker, A., McNamara, C., Henson, K., Kato, N., Kuhen, K., Nagle, A., Adrián, F., Matzen, J. T., Anderson, P., Nam, T.-G., Gray, N. S., Chatterjee, A., Janes, J., Yan, S. F., Trager, R., Caldwell, J. S., Schultz, P. G., Zhou, Y., and Winzeler, E. A. (2008) In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc. Natl. Acad. Sci. U. S. A. 105, 9059-9064
27. Bhakdi, S. C., Sratongno, P., Chimma, P., Rungruang, T., Chuncharunee, A., Neumann, H. P., Malasit, P., and Pattanapanyasat, K. (2007) Re-evaluating acridine orange for rapid flow cytometric enumeration of parasitemia in malaria-infected rodents. Cytometry A 71, 662-667
28. Jimenez-Diaz, M. B., Rullas, J., Mulet, T., Fernandez, L., Bravo, C., Gargallo-Viola, D., and Angulo-Barturen, I. (2005) Improvement of detection specificity of Plasmodium-infected murine erythrocytes by flow cytometry using autofluorescence and YOYO-1. Cytometry A 67, 27-36
29. Xie, L., Li, Q., Johnson, J., Zhang, J., Milhous, W., and Kyle, D. (2007) Development and validation of flow cytometric measurement for parasitaemia using autofluorescence and YOYO-1 in rodent malaria. Parasitology 134, 1151-1162
30. Inglese, J., Auld, D. S., Jadhav, A., Johnson, R. L., Simeonov, A., Yasgar, A., Zheng, W., and Austin, C. P. (2006) Quantitative high-throughput screening: a titration-based approach that efficiently identifies biological activities in large chemical libraries. Proc. Natl. Acad. Sci. U. S. A. 103, 11473-11478
31. Vinetz, J. M., Clain, J., Bounkeua, V., Eastman, R. T., and Fidock, D. A. (2011) Chemotherapy of malaria. In Goodman & Gilman's The Pharmacological Basis of Therapeutics (Brunton, L., Chabner, B., and Knollman, B., eds) pp. 1383-1418, McGraw Hill Medical, New York
32. Barthel, D., Schlitzer, M., and Pradel, G. (2008) Telithromycin and quinupristin-dalfopristin induce delayed death in Plasmodium falciparum. Antimicrob. Agents Chemother. 52, 774-777
33. Di, L., and Kerns, E. H. (2006) Biological assay challenges from compound solubility: strategies for bioassay optimization. Drug Discov. Today 11, 446-451
34. Nallan, L., Bauer, K. D., Bendale, P., Rivas, K., Yokoyama, K., Hornéy, C. P., Pendyala, P. R., Floyd, D., Lombardo, L. J., Williams, D. K., Hamilton, A., Sebti, S., Windsor, W. T., Weber, P. C., Buckner, F. S., Chakrabarti, D., Gelb, M. H., and Van Voorhis, W. C. (2005) Protein farnesyltransferase inhibitors exhibit potent antimalarial activity. J. Med. Chem. 48, 3704-3713
35. Carter, A. P., Clemons, W. M., Brodersen, D. E., Morgan-Warren, R. J., Wimberly, B. T., and Ramakrishnan, V. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407, 340-348
36. Janbon, M., Bertrand, A., and Pourquier, M. (1963) Kitasamycin: experimental in vitro studies and first clinical results. Gaz. Med. Fr. 70(Suppl.), 9-21
37. Barton, M. D. (2000) Antibiotic use in animal feed and its impact on human health. Nutr. Res. Rev. 13, 279-299
38. Van der Heyde, H. C., Elloso, M. M., vande Waa, J., Schell, K., and Weidanz, W. P. (1995) Use of hydroethidine and flow cytometry to assess the effects of leukocytes on the malarial parasite Plasmodium falciparum. Clin. Diagn. Lab. Immunol. 2, 417-425
39. Tuma, R. S., Beaudet, M. P., Jin, X., Jones, L. J., Cheung, C. Y., Yue, S., and Singer, V. L. (1999) Characterization of SYBR Gold nucleic acid gel stain: a dye optimized for use with 300-nm ultraviolet transilluminators. Anal. Biochem. 268, 278-288
40. Peters, W. (1965) Drug resistance in Plasmodium berghei Vincke and Lips, 1948. I. Chloroquine resistance. Exp. Parasitol. 17, 80-89
41. Wells, T. N., and Poll, E. M. (2010) When is enough enough? The need for a robust pipeline of high-quality antimalarials. Discov. Med. 9, 389-398
42. Kuo, M. R., Morbidoni, H. R., Alland, D., Sneddon, S. F., Gourlie, B. B., Staveski, M. M., Leonard, L., Gregory, J. S., Janjigian, A. D., Yee, C., Kreiswirth, B., Iwamoto, H., Perozzo, R., Jacobs, J. W. R., Sacchettini, J. C., and Fidock, D. A. (2003) Targeting tuberculosis and malaria through inhibition of enoyl reductase: compound activity and structural data. J. Biol. Chem. 278, 20851-20859
43. McLeod, R., Muench, S. P., Rafferty, J. B., Kyle, D. E., Mui, E. J., Kirisits, M. J., Mack, D. G., Roberts, C. W., Samuel, B. U., Lyons, R. E., Dorris, M., Milhous, W. K., and Rice, D. W. (2001) Triclosan inhibits the growth of Plasmodium falciparum and Toxoplasma gondii by inhibition of apicomplexan Fab I. Int. J. Parasitol. 31, 109-113
44. Waller, R. F., Keeling, P. J., Donald, R. G., Striepen, B., Handman, E., Lang-Unnasch, N., Cowman, A. F., Besra, G. S., Roos, D. S., and McFadden, G. I. (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 95, 12352-12357
45. Jomaa, H., Wiesner, J., Sanderbrand, S., Altincicek, B., Weidemeyer, C., Hintz, M., Turbachova, I., Eberl, M., Zeidler, J., Lichtenthaler, H. K., Soldati, D., and Beck, E. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285, 1573-1576
46. Olumese, P. (2010) Guidelines for the Treatment of Malaria. World Health Organization, Geneva, Switzerland
47. Kalilani, L., Mofolo, I., Chaponda, M., Rogerson, S. J., Alker, A. P., Kwiek, J. J., and Meshnick, S. R. (2007) A randomized controlled pilot trial of azithromycin or artesunate added to sulfadoxine-pyrimethamine as treatment for malaria in pregnant women. PLoS One 2, e1166
48. Chico, R. M., Pittrof, R., Greenwood, B., and Chandramohan, D. (2008) Azithromycin-chloroquine and the intermittent preventive treatment of malaria in pregnancy. Malar. J. 7, 255
49. Luntamo, M., Kulmala, T., Mbewe, B., Cheung, Y. B., Maleta, K., and Ashorn, P. (2010) Effect of repeated treatment of pregnant women with sulfadoxine-pyrimethamine and azithromycin on preterm delivery in Malawi: a randomized controlled trial. Am. J. Trop. Med. Hyg. 83, 1212-1220
50. Tan, K. R., Magill, A. J., Parise, M. E., and Arguin, P. M. (2011) Doxycycline for malaria chemoprophylaxis and treatment: report from the CDC expert meeting on malaria chemoprophylaxis. Am. J. Trop. Med. Hyg. 84, 517-531
51. Friesen, J., Silvie, O., Putrianti, E. D., Hafalla, J. C., Matuschewski, K., and Borrmann, S. (2010) Natural immunization against malaria: causal prophylaxis with antibiotics. Sci. Transl. Med. 2, 40ra49
52. Okamoto, N., Spurck, T. P., Goodman, C. D., and McFadden, G. I. (2009) Apicoplast and mitochondrion in gametocytogenesis of Plasmodium falciparum. Eukaryot. Cell. 8, 128-132
53. Noedl, H. (2009) ABC - antibiotics-based combinations for the treatment of severe malaria? Trends Parasitol. 25, 540-544
54. Berkley, J., Mwarumba, S., Bramham, K., Lowe, B., and Marsh, K. (1999) Bacteraemia complicating severe malaria in children. Trans. R. Soc. Trop. Med. Hyg. 93, 283-286
55. Berkley, J. A., Lowe, B. S., Mwangi, I., Williams, T., Bauni, E., Mwarumba, S., Ngetsa, C., Slack, M. P., Njenga, S., Hart, C. A., Maitland, K., English, M., Marsh, K., and Scott, J. A. (2005) Bacteremia among children admitted to a rural hospital in Kenya. N. Engl. J. Med. 352, 39-47
56. Dharia, N. V., Sidhu, A. B., Cassera, M. B., Westenberger, S. J., Bopp, S. E., Eastman, R. T., Plouffe, D., Batalov, S., Park, D. J., Volkman, S. K., Wirth, D. F., Zhou, Y., Fidock, D. A., and Winzeler, E. A. (2009) Use of high-density tiling microarrays to identify mutations globally and elucidate mechanisms of drug resistance in Plasmodium falciparum. Genome Biol. 10, R21
57. Eastman, R. T., Dharia, N. V., Winzeler, E. A., and Fidock, D. A. (2011) Piperaquine resistance is associated with a copy number variation on chromosome 5 in drug-pressured Plasmodium falciparum parasites. [Epub ahead of print] Antimicrob. Agents Chemother. PMID: 21576453
58. AlKadi, H. O. (2007) Antimalarial drug toxicity: a review. Chemotherapy 53, 385-391
59. Schoepflin, S., Lin, E., Kiniboro, B., DaRe, J. T., Mehlotra, R. K., Zimmerman, P. A., Mueller, I., and Felger, I. (2010) Treatment with coartem (artemether-lumefantrine) in Papua New Guinea. Am. J. Trop. Med. Hyg. 82, 529-534